59 THE SIGNIFICANCE OF SIDEROPHORES IN SOIL

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of bacteria, fungi and plants. There are numerous factors influencing the production of siderophores by soil microorganisms, for instance pH. Due to the fact that ...
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THE SIGNIFICANCE OF SIDEROPHORES IN SOIL Anna Grobelak, Joanna Hiller Politechnika Częstochowska, Wydział Inżynierii Środowiska i Biotechnologii, Instytut Inżynierii Środowiska Opiekun naukowy: prof. dr hab. inż. Małgorzata Kacprzak

Abstract: Sideropores are defined as relatively low molecular weight iron ion specific chelating agents, which existence is dependent on the amount of iron in the soil. Iron is known to be a very important microelement influencing metabolic processes of bacteria, fungi and plants. There are numerous factors influencing the production of siderophores by soil microorganisms, for instance pH. Due to the fact that the existence of different iron forms in the soil is strictly connected with pH, the absorption of iron by bacteria or fungi differs. Siderophores have very special function, especially when they are produced by bacteria living in the root zone, which are known as PGPR (Plant Growth Promoting Rhizobacteria) on the basis of the fact that their metabolites influence the growth and development of green plants in case of iron deficiency. One of the most important examples of PGPR, and the best known one, is Pseudomonas fluorescence, which contribution to plant growth has been tested in various research. These chelating agents also cause the absorption of heavy metals from the soil, which can be very positive when it comes to bioaugmentation of soils contaminated with heavy metals. 1. Introduction Nowadays, according to a rapid technological and industrial development, more and more attention is being given not only to ecology, which is the basis for healthy and productive life, but also to a wide variety of methods of increasing crops, as well as their nutritious properties. Consequently, there have been numerous tests and research carried out recently aiming at determining the most adequate conditions for certain plants growth in numerous ecosystems, obtaining the most effective and rich in essential elements and nutrients means of food [ Meera and Balabaskar, 2012, Alvarez et al. 1994]. Among the most valid factors contributing to plant growth and development of fungi and bacteria, PGPR (called Plant Growth Promoting Rhizobacteria owing to their existence close to plant roots), play a very significant role. PGPR were first defined by Kloepper and Schroth as soil bacteria "that colonize the roots of plants following inoculation onto seed and that enhance plant growth" [Nelson, 2004]. They influence, directly or indirectly, on the ability to survive in response to seed exudates [Nelson, 2004]. There are diverse groups of microbes in rhizosphere which are known to stimulate plant growth, mainly by increased uptake of nitrogen, iron and phosphorus, as well as by controlling plant diseases [Adler et al., 2012]. Consequently, due to their diversity colonization ability, mechanisms of action, formulation and application, they are able to facilitate their environment, and thus provide components essential in the process of plant development. Plant growth is influenced by both abiotic and biotic factors and rhizosphere supports active microbial populations capable of exerting neutral but beneficial effects contributing to plant growth, which influences the maintenance of root health, nutrient uptake as well as plant tolerance of environmental stress, occuring where there is insufficient amount of valid substance supporting basic life functions and

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growth. In a case when in the environment there can be observed a noticable loss of iron, bacterias and fungi existing in the root zone produce different secondary metabolitices, such as siderophores. Siderophores are definied as relatively low molecular weight, iron ion specific chelating agents elaborated by bacteria and fungi growing under low iron stress.[Neilands, 1995; Balagurunathan and Radhakrishnan, 2007]. That mechanism is essential in almost all aerobic and facultative anaerobic microbes, which produce at least one siderophore [Neilands, 1995]. Iron is a very essential microelement for all forms of life and each organism growing under aerobic conditions requires iron for numerous functions, the most important of which are oxygen reduction (ATP synthesis), reduction of ribotide pecursors of DNA and heme formation. For optimum growth, at least one micromolar iron is needed [Neilands, 1995; Krey, 2000], nevertheless there is not enough iron in soil to provide it for all organisms living there [Joshi et al., 2006], which is partially connected with neutral soil pH (7,0), usually being far below growth requirement of most microorganisms. It has been estimated that suitable iron exists in soils in concentration of 10-17 M or 10-18 M [Joshi et al., 2006; Khan, 2005; Prasad et al. 2011]. In a situation when conditions are limited for iron presence, some fungi and bacteria synthesize and secrete siderophores, and thus bind ferric iron with high affinity. Primarily, they can bind iron from weaker ferric siderophores or from other species, therefore they play a role of mediators of competitive interactions among organisms [Khan et al., 2005]. 2. Description of issues Siderophores produced by microorganisms There are about 500 different siderophores [Illmer and Buttinger, 2005] distinguished, which are produced either by fungi or by facultative anaerobic bacteria. Phyto-siderophores are plants analogous chelating agents, nevertheless there is no similar structure in animal tissues[Illmer and Buttinger, 2005] When it comes to molecular weights, chemically, siderophores do not exceed 1500 Dalton and they can be divided into the catechols and hydroxamates, carboxalate [Illmer and Buttinger, 2005; Ali and Vidhale, 2013]. Despite the fact that the synthesis of siderophores is strictly connected with an available iron there is also some concentration of iron needed for inhibitation of siderophores [Sayyed et al., 2004]. The main two kinds of siderophores are bacteria and fungi siderophores. Bacteria and fungi produce hydroxymate siderophore, most of which are present in the form of C (=O)N-9OH)R, where R can be either an amino-acid or derovative [Ali and Vidhale, 2013]. To oxygen molecules are provided by each hydroxymate groups and they form bidenatate ligand with iron [Ali and Vidhale, 2013]. In this way, siderophores forms hexadentate octanhendral complex with Fe3+. The typical absorption of siderophores when they bound to iron is usually between 425 and 500 nm. It is typical for catecholate group to provide two oxygen atoms or chelation with iron [Ali and Vidhale, 2013; Balagurunathan and Radhakrishnan, 2007]. Hexadentate octahedral complex is formed in hydrixymate siderophores [Ali and Vidhale, 2013]. We can distinguish linear catecholate siderophores produced in certain species, for instance Agrobactin which is produced by Agrobacterium tumefaciens or a mix catecholatehydroxamate siderophore produced by Pseudomonas [Ali and Vidhale, 2013]. Carboxylate(complexones) are characterised by rhizobactin which is produced by Rhizobium meliloti strain is amino poly (carboxylic acid) with ethylenediaminedicarboxyl and hydroxycarboxyl as iron-chelating groups. They are neither catecholates nor hydroxamates but a class of complexion siderophores [Ali and Vidhale, 2013].

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There are about 100-150 main fungal siderophores and the major class includes ferrichromes, [Winkelmann, 2007]. The group consists of 20 structurally different hexapeptides, nevertheless fungi can produce a set of different siderophore apart from the already mentioned ones in order to cover the range of physico-chemical properties [Winkelmann, 2007]. Ferrichromes have received the highest level of structural development because they consist of cyclic hexapeptides, which are largely resistant to environmental degradation [Winkelmann, 2007]. It is the major siderophores which was isolated as a growth factor for other microorganisms from the fungus Ustilago spohaerogena and it is known to be hydroxymate [Ali and Vidhale, 2013]. Siderophores in the soil Despite great variety of siderophores which can be found in environment various encouraging and discouraging factors play a huge role when it comes to their presence. There is competition between some microorganisms which may have extremely negative impact on siderophores exsistance in the soil. Ferrichromes are known to be very resistance to degradation owing to the fact that they are generally resistant to rapid enzymatic degradation, especially when they are in the form of the ferric complexes. A key factor in the process is the presence of certain enzymes, produced not only other microorganisms but also by plants. When fine roots or root hairs of plants are colonized by various bacteria present in soil, the situation of iron deficiency does not constitute a serious problem for the growth of both organisms because siderophores are ready to provide the adequate and necessary amount of iron on the basis of tight association in a form of symbiosis. For this reason, siderophores production by root nodule bacteria and fungi is more important for survival and plant growth organisms in competitive soil environment deficient in iron [Khan et al. 2005; Winkelmann, 2007]. The mechanism of siderophores activity Aerobactin is the siderophore of which biosynthesis is usually described as it was the first one to be isolated and therefore, it can provide the greatest amount of information concerning biosynthesis. There are four gene products required for this process, however, the gene code encoding monooxygenase is most important due to the fact that this enzyme catalysis the first step in the pathway and plays a major role in blocking aerobacting synthesis in chomethearpeuthic intervention [Falguni et al., 2006]. There are two main pathways of siderophore biosynthesis, the first one of which is directed by a large family of modular multi enzymes, which are called non-ribosomal peptide synthetases (NRPSs). The second type as known as NRPS independent, which are not synthesise in ribosomes [Barry, 2009; Crosa et al., 2002]. In the process of transport system, there have been identified three main siderophores transport genes - TAF1, ENB1 and ARN1, which are the major facilitators family by deletion of the transporter genes in fungi. These siderophores transport is dependent on proton gradient and cell wall material is also involved in iron transport [Winkelmann, 2007]. The process of iron uptake in microorganisms is both a receptordependent and energy dependent. Because siderophores are a part of multi-component system for transporting iron into a cell. Among other components we can provide a specific outer membrane receptor protein Fec A, Fep A and TonB-ExbB-ExbD protein complex, which can be found in the inner membrane. In case of low iron efficency, bacteria synthezise siderophores and increase number of receptors modules when siderophores excerate outside of cell through membrane receptor and binds with iron complex in order to transport it into the cell via outer membrane receptor. There are two major proteins which span the membrane an act as a permease as well as provide energy

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for transport. Iron complex is realesed in cythoplasm with the help of special proteins [Ali and Vidhale, 2013]. It has been reported the transcription of iron regulated gene is under the negative control of four protein, which is a repressor with Fe2+, as an essential compressor [Sayyed et al., 2004]. The factors influencing siderophores production Soil pH plays a very significant role in solubility of iron and is also linked with the growth of organisms. Along with pH increasing towards alkalinity, the production of siderophores is ceasing due to the fact that alkaline pH enables excess solubilization of iron, leading to the increase in the soil [Sayyed et al., 2004] One of the most important ecological factors essential for biosynthesis is external pH owing to the fact that it is essential in the soilubility of iron and thus, influences growing organisms. It has been estimated that when pH is neutral (7,0) the production of siderophores is the greatest as it is linked with iron defficency, constituting at the same time, the best breeding condition for bacteria [Sayyed et al., 2004]. When pH increases, the production of siderophores reduces [ Sayyed et al., 2004]. pH is also a key factor in regulating biosynthesis which is connected with Fe-depending regulation system. It can be explained by a protective role of siderophore- downregulation occurring along with decreasing pH when many potential toxic metals are available and can be taken up with siderophores. Consequently, the presence or the lack of iron as well as its concentration is very meaningful when it comes to siderophores concentration, similarly, it also influences toxic metal absorption [Illmer and Buttinger, 2005]. The requirement of iron for cellular processes of organisms is reflected in iron concentration because at about 20 uM of iron, there is no production of siderophores, which suggest iron sufficency in organisms [Sayyed et al., 2004]. Siderophore production is observed to increase, as well as the growth of cultures, when Pb is present in the soil, while Mn, Hg and Co have inhibitory effect on growth and siderophore production. Fe2+ may be substituted with Mn2+ Zn2+ in intercellular control of siderophores synthesis [Sayyed et al., 2004]. The presence of Al also attributes to siderophores production while iron is a limiting factor, in particular the synthesis of Rhizobium increased by such an addition of 100 uM Al3+[Illmer and Buttinger, 2005]. The importance of siderophores on plant growth PGPR play different functions, which depend on the environment they can be found in as well as its diversity and special needs required not only by bacteria and fungi but also by other plants co-existing with them. The major function which is essential for plant growth is the production of siderophores which assimilate Fe from environment for their own purpose or to be used by the plants living in the symbiosis with them. It is especially essential in the time of environment stress resulting from the inadequate amount of iron in the soil, which main lead to the inhibition of plant growth as well as disturbing their functions. Most research into siderophores is carried out on the example Pseudomonas which is known to be the most typical and representant of PGPR [Sayyed et al., 2004]. It has been proved that siderophores associated with certain plant life have direct or indirect impact on their growth through control of noxius organisms in the soil. Iron insensitive enzyme complex, nitrogenase, found in Rhizobium may require an intact siderophore system for expression of prokaryotic catalyst Neilands, 1995]. According to Kloepper, Pseudomonas, which produce psedubactin increase growth and yield of various plants in agriculture inoculation of soil. Among the activities that promote production of HCN, siderophores, protease antimicrobials, phosphate solubilizing enzymes can be found [Ali and Vidhale, 2013]. In aquatic environments, most frequently present siderophores are hydromaxate which are known for their accumulation of heavy

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metals and toxines from plants and contaminated soil, which results in decreased soil microbial activity and soil fertility. Burton has found out that some microbes synthesise siderophores while others use them without synthesising first. Similarly, many bacteria supports the growth of microorganisms by production of siderophore, antibiotics and cyanide, therefore it can be said that siderophores are inhibitors of various fungi. Some direct correlation between siderophore synthesis and Pseudomonas fluroescence has also been detected, which indicates their capacity to inhibit germination of chlamydospores of Fusarium oxysporum. Mutants incapable of producing some siderophores, like pyoverdineare, reduced in captifity in order to intensify different plant phatogens, as it also happens in antibiotics [Ali and Vidhale, 2013]. Consequently, it has been observed that plant pathogens can be used as a way of biological control as a potential nonchemical means, which is a relatively cheap and effective, eco-friendly method of the management of crop diseases [Meera and Balabaskar, 2012]. Bacteria living in the vicinity of root zones, produce various antibiotics, which aim is to increase the chances for their survival in competitive environment. These antibiotics can be used by co-existing in symbiothic plants and thus, it has a direct impact on their immunity to diseases; consequently, it increases plant growth as well as crop efficiency [Meera and Balabaskar, 2012]. 3. Summary Among all elements exiting in environment supporting plant and microorganisms life, iron is one of the most important microelement necessary for all living cells. Due to the fact that iron characterizes with poor soilubilty, it is very difficult to take it up into cells [Ali and Vidhale, 2013; Crosa and Walsh, 2002 ]. Therefore, in order to supply all living cells with iron, some bacteria, fungi and algea produce iron chelator, siderophores outside the cells and ferric iron chealtes the siderophores. The application of the microbial siderophores is essential and of an enormous scope not only for plants but also for humans and animals. At present, it is most frequently use in agricultural, clinical and environmental area, as well as for microbiology research carried out in laboratories [Ali and Vidhale, 2013]. Another aspect worth mentioning while discussing siderophores functions is their positive activity associated with the absorption of heavy and toxic metals which are natural components in soil. The most frequently heavy metal contaminants to be found in plant environment are Cd, Cr, Cu, Hg, Pb, Ni. Unfortunately, pollution of biosphere by toxic metal has been increasing dramatically since the beginning of industrial revolution and it is constantly on the go. The chances for improvement in this area are limited due to industrialization on a huge scale [Ali and Vidhale, 2013; Balagurunathan and Radhakrishnan, 2007]. Heavy metal contamination can not only be found in soil but also in water ecosystem, which has a direct and indirect influence on human life and health [Ali and Vidhale, 2013]. Siderophores are natural regulators of ecosystems, which is especially important when we consider their usage to treating radioactive areas or highly contaminated soil and water environments. There is a need to carry out more research into siderophores which have not been distinguish from marine ecosystems such as deep sees and oceans, dessert and forested areas so as to determine their functions and gain more knowledge into functions [Ali and Vidhale, 2013]. On the basis of the fact that the advantage to be taken from siderophore for agriculture and activity themselves it can be assumed ,by doing so, we can influence plant growth to a great extent. Acknowledgements The project was supported through funding from No NCN-UMO-2011/03/N/NZ9/02034

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4. References Adler C., Natalia S. Corbalán, Mohammad R. Seyedsayamdost, María Fernanda Pomares, Ricardo E. de Cristóbal, Jon Clardy, Roberto Kolter,Paula A. Vincent, 2012. Catecholate Siderophores Protect Bacteria from Pyochelin Toxicity. DOI: 10.1371/journal.pone.0046754 Balagurunathan R., M. Radhakrishnan, 2007. Microbal siderophores - gateway for iron removal. ENVIS CENTRE Newsletter Vol.5, July 2007. Barry Sarah.M., Volume 13, Issue 2, Gregory L.Challis, 2009. Recent advances in siderophore biosynthesis. Current Opinion in Chemical Biology, April 2009, Pages 205–215. Crosa Jorge H., and Christopher T. Walsh, 2002. Genetics and Assembly Line Enzymology of Siderophore Biosynthesis in Bacteria. Microbiol Mol Biol Rev. 2002 June; 66(2): 223–249. Falguni R. Joshi, Swati P. Kholiya, G. Archana, Anjana Desai, 2006. Siderophore cross-utilization amongst nodule isolates of the cowpea miscellany group and its effect on plant growth in the presence of antagonistic oranisms. Microbiological Research 163 (2008) 564-570. Illmer Paul, Rudolf Buttinger, 2005. Interactions between iron availability, aluminium toxicity and fungal siderophores. BioMetals (2006) 19:367–377. Khan Arif, R. Geetha ,Aparna Akolkar, Ami Pandya,G. Archana, Anjana J. Desai, 2005. Differential cross-utilization of heterologous siderophores by nodule bacteria of Cajanus cajan and its possible role in growth under iron-limited conditions. Soil Ecology 34 (2006) 19–26. Krey Whitney B., 2005. Siderophore Production by Heterotrophic Bacterial Isolates from the Costa Rica Upwelling Dome. Ma Y., M.N.V. Prasad, M. Rajkumar, H. Freitas, Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnology Advances 29 (2011) 248–258. Marcos A. De Brito Alvarez, Serge Gagne, Hani Antoun, 1994. Effect of Compost on Rhizosphere Microflora of the Tomato and on the Incidence of Plant Growth-Promoting Rhizobacteria. Applied and Environmental Microbiology, Jan. 1995, p. 194–199. Meera T. and P. Balabaskar, 2012. Isolation and characterization of Pseudomonas fluorescens from rice fields. International Journal of Food, Agriculture and Veterinary Sciences. http://www.cibtech.org/jfav.htm 2012 Vol. 2 (1) January-April, pp.113120/Meera and Balabaskar Neilands J. B., 1995. Siderophores: Structure and Function of Microbal Iron Transport Compounds. The Journal of Biological Chemistry, 1995, 270: 26723-26726. Nelson Louise M., 2004. Plant Growth Promoting Rhizobacteria (PGPR): Prospects for New Inoculants. Online. Crop Management doi:10.1094/CM-2004-0301-05-RV. Sajeed Syed Ali and N.N. Vidhale, 2013. Bacterial Siderophore and their Application: A review. International Journal of Current Microbiology and Applied Science vol. 2 number 12 (2013) pp. 303-312. Sayyed R. Z. ,M.D. Badgujar, H.M. Sonawane, M.M.Mhaske and S.B.Chincholkar, 2004. Production of microbial iron chealtora (siderophores) by fluorescent Pseudomonas. Indian Journal of Biotechnology vol. 4, October 2005, pp 484-490. Winkelmann Gunther, 2007. Ecology of siderophores with special reference to the fungi. Biometals (2007) 20:379–392. http://darchive.mblwhoilibrary.org:8080/bitstream/handle/1912/2394/Krey_thesis.pdf?seq uence=1 : Adres do korespondencji: [email protected]

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